S-adenosyl-L-methionine:magnesium-protoporphyrin IX O-methyltransferase from Rhodobacter capsulatus: Mechanistic insights and stimulation with phospholipids

Biochemical Journal

Volumn 406, Issue 3, 2007, Pages 469-478

  Sawicki, Artur ^a   Willows, Robert D ^a  

^a MACQUARIE UNIVERSITY   (Australia)

Author keywords

Bacteriochlorophyll biosynthesis; BchM; Magnesium chelatase; Methyltransferase; Phosphatidylglycerol; Rhodobacter capsulatus

Indexed keywords

BACTERIOCHLOROPHYLL BIOSYNTHESIS; MAGNESIUM CHELATASE; METHYLTRANSFERASE; PHOSPHATIDYLGLYCEROLS; RHODOBACTER CAPSULATUS;

BIOSYNTHESIS; CHLOROPHYLL; IN SITU PROCESSING; PHOSPHOLIPIDS; POLYPEPTIDES;

ENZYMES;

COBALT; DEUTEROPORPHYRIN DERIVATIVE; MAGNESIUM; MAGNESIUM CHELATASE; MAGNESIUM DERIVATIVE; METALLOPORPHYRIN; METHIONINE SYNTHASE; PHOSPHOLIPID; POLYSORBATE 20; PROTOPORPHYRIN; S ADENOSYLMETHIONINE; SURFACTANT; UNCLASSIFIED DRUG; ZINC;

AFFINITY CHROMATOGRAPHY; ARTICLE; BACTERIAL METABOLISM; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; GEL PERMEATION CHROMATOGRAPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RHODOBACTER CAPSULATUS;

ENZYME ACTIVATION; KINETICS; METHYLTRANSFERASES; PHOSPHOLIPIDS; PROTOPORPHYRINS; RHODOBACTER CAPSULATUS; S-ADENOSYLMETHIONINE;

ESCHERICHIA COLI; RHODOBACTER CAPSULATUS;

EID: 34548726734     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20070284     Document Type: Article

References (63)

1. Gregor, J. and Klug, G. (1999) Regulation of bacterial photosynthesis genes by oxygen and light. FEMS Microbiol. Lett. 179, 1-9
2. Biel, A. J. and Marrs, B. L. (1983) Transcriptional regulation of several genes for bacteriochlorophyll biosynthesis in Rhodobacter capsulatus. J. Bacteriol. 156, 686-694
3. Zsebo, K. M. and Hearst, J. E. (1984) Genetic-physical mapping of a photosynthetic gene cluster from R. capsulata. Cell 37, 937-947
4. Taylor, D. P., Cohen, S. N., Clark, W. G. and Marrs, B. L. (1983) Alignment of genetic and restriction maps of the photosynthesis region of the Rhodopseudomonas capsulata chromosome by a conjugation-mediated marker rescue technigue. J. Bacteriol. 154, 580-590
5. Yen, H.-C. and Marrs, B. L. (1976) Map of genes for carotenoid and bacteriochlorophyll biosynthesis in Rhodopseudomonas capsulata. J. Bacteriol. 126, 619-629
6. Marrs, B. (1981) Mobilization of the genes for photosynthesis from Rhodopseudomonas capsulata by a promiscuous plasmid. J. Bacteriol. 146, 1003-1012
7. Alberti, M., Burke, D. H. and Hearst, J. E. (1995) Structure and sequence of the photosynthetic gene cluster. In Anoxygenic Photosynthetic Bacteria, (Blankenship, R. E., Madigan, M. T. and Bauer, C. E., eds), pp.1083-1106, Kluwer Academic Publishing, Amsterdam
8. Yang, Z. and Bauer, C. E. (1990) Rhodobacter capsulatus genes involved in early steps of the bacteriochlorophyll biosynthetic pathway. J. Bacteriol. 172, 5001-5010
9. Bollivar, D. W., Jiang, Z.-Y., Bauer, C. E. and Beale, S. I. (1994) Heterologous expression of the BchM gene product from Rhodobacter capsulatus and demonstration that it encodes S-adenosyl-L-methionine:Mg-protoporphyrin IX methyltransferase. J. Bacteriol. 176, 5290-5296
10. Gibson, L. S. D. and Hunter, C. N. (1994) The bacteriochlorophyll biosynthesis gene, bchM, of Rhodobacter sphaeroides encodes S-adenosyl:Mg protoporphyrin IX methyltransferase. FEBS Lett. 352, 127-130
11. Beale, S. I. (1999) Enzymes of chlorophyll biosynthesis. Photosynthesis Res. 60, 43-73
12. Beale, S. I. and Weinstein, J. D. (1990) Tetrapyrrole metabolism in photosynthetic organisms. In Biosynthesis of Heme and Chlorophylls (Dailey, H.A., ed.), pp. 287-391, McGraw-Hill Publishing, New York
13. Willows, R. D. (2003) Biosynthesis of chlorophylls from protoporphyrin IX. Natural Products Reports 20, 1-16
14. Bollivar, D. W. (2006) Recent advances in chlorophyll biosynthesis. Photosynthesis Res. 89, 1-22
15. Bollivar, D. W. (2003) Intermediate steps in chlorophyll biosynthesis methylation and cyclization. In The Porphyrin Handbook, Chlorophylls and Bilins: Biosynthesis, Synthesis, and Degradation (Kadish, K.M., Smith, K.M., Guilard, R., eds), pp. 49-69, Academic Press, Sydney
16. Pontier, D., Albrieux, C., Joyard, J., Lagrange, T. and Block, M. A. (2007) Knock-out of the magnesium protoporphyrin IX methyltransferase gene in Arabidopsis: effects on chloroplast development and on chloroplast-to-nucleus signaling. J. Biol. Chem. 282, 2297-2304
17. Nott, A., Jung, H.-S., Koussevitzky, S. and Chory, J. (2006) Plastid-to-nucleus retrograde signaling. Ann. Rev. Plant Biol. 57, 739-759
18. Ellsworth, R. K. and Dullaghan, J. P. (1972) Activity and properties of S-adenosyl-L-methionine:magnesium-protoporphyrin IX methyltransferase in crude homogenates from wheat seedlings. Biochim. Biophys. Acta 268, 327-333
19. Ellsworth, R. K., Dullaghan, J. P. and St Pierre, M. E. (1974) The reaction mechanism of S-adenosyl-L-methionine:magnesium protoporphyrin IX methyltransferase of wheat. Photosynthetica 8, 375-383
20. Gibson, K. D., Neuderger, A. and Tait, G. H. (1963) Studies on the biosynthesis of porphyrin and bacteriochlorophyll by Rhodopseudomonas spheroides. Biochem. J. 88, 325-334
21. Hinchigeri, S. B., Chan, J. C.-S. and Richards, W. R. (1981) Purification of S-adenosyl-L-methionine:magnesium protoporphyrin IX methyltransferase by affinity chromatography. Photosynthetica 15, 351-359
22. Hinchigeri, S. B., Nelson, D. W. and Richards, W. R. (1984) The purification and reaction mechanism of S-adenosyl-L-methionine: magnesium protoporphyrin IX methyltransferase from Rhodopseudomonas sphaeroides. Photosynthetica 18, 168-178
23. Hinchigeri, S. B. and Richards, W. R. (1982) The reaction mechanism of S-adenosyl-L-methionine:magnesium protoporphyrin IX methyltransferase from Euglena gracilis. Photosynthetica 16, 554-560
24. Shepherd, M. and Hunter, C. N. (2004) Transient kinetics of the reaction catalysed by magnesium protoporphyrin IX methyltransferase. Biochem. J. 382, 1009-1013
25. Shepherd, M., Reid, J. D. and Hunter, C. N. (2003) Purification and kinetic characterization of the magnesium protoporphyrin IX methyltransferase from Synechocystis PCC6803. Biochem. J. 371, 351-360
26. Shieh, J., Miller, G. W. and Psenak, M. (1978) Properties of S-adenosyl-L-methionine magnesium-protoporphyrin IX methyltransferase from barley. Plant Cell Physiol. 19, 1051-1059
27. Yee, W. C., Eglsaer, S. J. and Richards, W. R. (1989) Confirmation of a ping-pong mechanism for S-adenosyl-L-methionine:magnesium protoporphyrin methyltransferase of etiolated wheat by an exchange reaction. Biochem. Biophys. Res. Commun. 162, 483-490
28. Smith, C. A., Suzuki, J. Y. and Bauer, C. E. (1996) Cloning and characterization of the chlorophyll biosynthesis gene chlM from Synechocystis PCC6803 by complementation of a bacteriochlorophyll biosynthesis mutant of Rhodobacter capsulatus. Plant Mol. Biol. 30, 1307-1314
29. Ebbon, J. G. and Tait, G. H. (1969) Studies on S-adenosyl- magnesium protoporphyrin methyltransferase in Euglena gracilis strain Z. Biochem. J. 111, 573-582
30. Block, M. A., Tewari, A. K., Albrieux, C., Maréchal, E. and Joyard, J. (2002) The plant S-adenosyl-L-methionine:Mg- protoporphyrin IX methyltransferase is located in both envelope and thylakoid chloroplast membranes. Eur. J. Biochem. 269, 240-248
31. Walker, C. J. and Willows, R. D. (1997) Mechanism and regulation of Mg-chelatase. Biochem. J. 327, 321-333
32. Willows, R. D. and Hansson, M. (2003) Mechanism, structure, and regulation of magnesium chelatase. In The Porphyrin Handbook (Kadish, K.M., Smith, K.M. and Guilard, R., eds), pp. 1-47, Academic Press, Sydney
33. Vale, R. D. (2000) AAA proteins: lords of the ring. J. Cell Biol. 150, F13-F19
34. Willows, R. D., Gibson, L. C. D., Kanangara, G. C., Hunter, C. N. and von Wettstein, D. (1996) Three separate proteins constitute the magnesium chelatase of Rhodobacter sphaeroides. Eur. J. Biochem. 235, 438-443
35. Gorchein, A. (1972) Magnesium protoporphyrin chelatase activity in Rhodopseudomonas sphaeroides: studies with whole cells. Biochem. J. 127, 97-106
36. Hinchigeri, S. B., Hundle, B. and Richards, W. R. (1997) Demonstration that the BchH protein of Rhodobacter capsulatus activates S-adenosyl-methionine:magnesium protoporphyrin IX methyltransferase. FEBS Lett. 407, 337-342
37. Jensen, P. E., Gibson, L. C. D., Shepherd, F., Smith, V. and Hunter, C. N. (1999) Introduction of a new branchpoint in tetrapyrrole biosynthesis in Escherichia coli by co-expression of genes encoding the chlorophyll-specific enzymes magnesium chelatase and magnesium protoporphyrin methyltransferase. FEBS Lett. 455, 349-354
38. Shepherd, M., McLean, S. and Hunter, C. N. (2005) Kinetic basis for linking the first two enzymes of chlorophyll biosynthesis. FEBS J. 272, 4532-4539
39. Alawady, A., Reski, R., Yaronskaya, E. and Grimm, B. (2005) Cloning and expression of the tobacco CHLM sequence encoding Mg protoporphyrin IX methyltransferase and its interaction with Mg chelatase. Plant Mol. Biol. 57, 679-691
40. Alawady, A. E. and Grimm, B. (2005) Tobacco Mg protoporphyrin IX methyltransferase is involved in inverse activation of Mg porphyrin and protoheme synthesis. Plant J. 41, 282-290
41. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
42. Willows, R. D. and Beale, S. I. (1998) Heterologous expression of the Rhodobacter capsulatus Bchl, D and H genes that encode magnesium chelatase subunits and characterization of the reconstituted enzyme. J. Biol. Chem. 273, 34206-34213
43. Reference deleted
44. Boyle, S. M., Markham, G. D., Hafner, E. W., Wright, J. M., Tabor, H. and Tabor, C. W. (1984) Expression of the cloned genes encoding the putrescine biosynthetic enzymes and methionine adenosylmethyltransferase of Escherichia coli speA, speB, speC and metK. Gene 30, 129-136
45. Markham, G. D., Hafner, E. W., Tabor, C. W. and Tabor, H. (1980) S-Adenosylmethionine synthetase from Escherichia coli. J. Biol. Chem. 255, 9082-9092
46. Schägger, H. and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379
47. Fuhrhop, J. and Granick, S. (1971) Magnesium protoporphyrin dimethyl ester and the dipotassium salt of magnesium protoporphyrin. Biochemical Preparations 13, 55-58
48. Falk, J. E. (1964) Laboratory methods. In Porphyrins and Metalloporphyrins: Their General, Physical And Coordination Chemistry, And Laboratory Methods, pp. 135-141, Elsevier Publishing Company, New York
49. Brisbin, D. A. and Richards, G. D. (1972) Kinetics of the reaction of some first-row transition metals with protoporphyrin IX dimethyl ester. Inorg. Chem. 11, 2849-2851
50. Karger, G. A., Reid, J. D. and Hunter, C. N. (2001) Characterization of the binding of the deuteroporphyrin IX to the magnesium chelatase H subunit and spectroscopic properties of the complex. Biochemistry 40, 9291-9299
51. Dalziel, K. (1959) Porphyrins and related compounds. In Data for Biochemical Research (Dawson, R.M. C., Elliott, D.C., Elliott, W.H. and Jones, K.M., eds), pp. 134, Oxford University Press, London
52. Loach, P. A. and Calvin, M. (1963) Oxidation states of manganese hematoporphyrin IX in aqueous solution. Biochemistry 2, 361-371
53. Ellsworth, R. K. and Murphy, S. J. (1978) Enzymatic preparation of Mg-protoporphyrin IX monomethyl ester. Photosynthetica 12, 81-82
54. Osborn, M. J. and Rothfield, L. I. (1966) Formation of lipopolysaccharide in mutant strains of Salmonella typhimurium. Methods Enzymol. 8, 456-466
55. Burton, K. (1959) Spectral data and pK values for purines, pyrimidines, nucleosides and nucleotides. In Data for Biochemical Research. (Dawson, R.M.C., Elliott, D.C., Elliott, W.H. and Jones, K.M., eds), pp. 74, Oxford University Press, London
56. Opekarová, M. and Tanner, W. (2003) Specific lipid requirements of membrane proteins: a putative bottleneck in heterologous expression. Biochim. Biophys. Acta 1610, 11-22
57. Russell, N. J. and Harwood, J. L. (1979) Changes in the acyl lipid composition of photosynthetic bacteria grown under photosynthetic and non-photosynthetic conditions. Biochem. J. 181, 339-345
58. Tait, G. H. and Gibson, K. D. (1961) The enzymic formation of magnesium protoporphyrin monomethyl ester. Biochim. Biophys. Acta 52, 614-616
59. Sreerama, N. and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287, 252-260
60. Cleland, W. W. (1963) The kinetics of enzyme-catalyzed reactions with two or more substrates or products. I. Nomenclature and rate equations. Biochim. Biophys. Acta 67, 104-137
61. Radmer, R. J. and Bogorad, L. (1967) S-adenosyl-L-methionine:magnesium protoporphyrin methyltransferase, an enzyme in the biosynthetic pathway of chlorophyll in Zea mays. Plant Physiol. 42, 463-465
62. Falk, J. E. (1964) Further coordination by metalloporphyrins. In Porphyrins and Metalloporphyrins: Their General, Physical And Coordination Chemistry, And Laboratory Methods, pp. 41-66, Elsevier Publishing Company, New York
63. Scheidt, W. R. (2000) Systematics of the stereochemistry of porphyrins and metalloporphyrins. In The Porphyrin Handbook (Kadish, K. M., Smith, K. M. and Guilard, R., eds), pp. 49-112, Academic Press, Sydney